The lamin-A/C-LAP2α-BAF1 protein complex regulates mitotic spindle assembly and positioning

Journal of Cell Science

Volumn 128, Issue 15, 2015, Pages 2830-2841

  Qi, Ran ^a   Xu, Nan ^a   Wang, Gang ^a   Ren, He ^a   Li, Si ^a   Lei, Jun ^a   Lin, Qiaoyu ^a   Wang, Lihao ^a   Gu, Xin ^a   Zhang, Hongyin ^b   Jiang, Qing ^a   Zhang, Chuanmao ^a  

^a BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^b Ministry of Education Beijing   (China)

Author keywords

BAF1; Cell cycle; Lamin A C; LAP2; Spindle assembly; Spindle positioning

Indexed keywords

BAF1 PROTEIN; DYNEIN ADENOSINE TRIPHOSPHATASE; LAMIN A; LAMIN C; LAP2ALPHA PROTEIN; NUCLEAR PROTEIN; UNCLASSIFIED DRUG; BANF1 PROTEIN, HUMAN; DNA BINDING PROTEIN; LAMINA-ASSOCIATED POLYPEPTIDE 2; LMNA PROTEIN, HUMAN; MEMBRANE PROTEIN; SMALL INTERFERING RNA;

ACTIN FILAMENT; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DEPOLYMERIZATION; HELA CELL LINE; MICROTUBULE ASSEMBLY; MITOSIS; MITOSIS SPINDLE; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA INTERFERENCE; GENETICS; HUMAN; METABOLISM; MICROTUBULE; SPINDLE APPARATUS; TUMOR CELL LINE;

ACTIN CYTOSKELETON; CELL LINE, TUMOR; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; LAMIN TYPE A; MEMBRANE PROTEINS; MICROTUBULES; MITOSIS; NUCLEAR PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SPINDLE APPARATUS;

EID: 84974602527     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.164566     Document Type: Article

References (40)

1. Azoury, J., Lee, K. W., Georget, V., Rassinier, P., Leader, B. and Verlhac, M.-H. (2008). Spindle positioning in mouse oocytes relies on a dynamic meshwork of actin filaments. Curr. Biol. 18, 1514-1519.
2. Burke, B. and Stewart, C. L. (2002). Life at the edge: the nuclear envelope and human disease. Nat. Rev. Mol. Cell Biol. 3, 575-585.
3. Burke, B. and Stewart, C. L. (2006). The laminopathies: the functional architecture of the nucleus and its contribution to disease. Annu. Rev. Genome Hum. Gen. 7, 369-405.
4. Burke, B. and Stewart, C. (2013). The nuclear lamins: flexibility in function. Nat. Rev. Mol. Cell Biol. 14, 13-24.
5. Clarke, P. R. and Zhang, C. (2008). Spatial and temporal coordination of mitosis by Ran GTPase. Nat. Rev. Mol. Cell Biol. 9, 464-477.
6. Dechat, T., Korbei, B., Vaughan, O. A., Vlcek, S., Hutchison, C. J. and Foisner, R. (2000). Lamina-associated polypeptide 2α binds intranuclear A-type lamins. J. Cell Sci. 113, 3473-3484.
7. Fu,W., Tao,W., Zheng, P., Fu, J., Bian, M., Jiang, Q., Clarke, P. R. and Zhang, C. (2010). Clathrin recruits phosphorylated TACC3 to spindle poles for bipolar spindle assembly and chromosome alignment. J. Cell Sci. 123, 3645-3651.
8. Galli, M., Muñoz, J., Portegijs, V., Boxem, M., Grill, S.W., Heck, A. J. R. and van den Heuvel, S. (2011). aPKC phosphorylates NuMA-related LIN-5 to position the mitotic spindle during asymmetric division. Nat. Cell Biol. 13, 1132-1138.
9. Gesson, K., Vidak, S. and Foisner, R. (2014). Lamina-associated polypeptide (LAP)2α and nucleoplasmic lamins in adult stem cell regulation and disease. Semin. Cell Dev. Biol. 29, 116-124.
10. Grill, S. W. and Hyman, A. A. (2005). Spindle positioning by cortical pulling forces. Dev. Cell 8, 461-465.
11. Gruenbaum, Y., Margalit, A., Goldman, R. D., Shumaker, D. K. and Wilson, K. L. (2005). The nuclear lamina comes of age. Nat. Rev. Mol. Cell Biol. 6, 21-31.
12. Güttinger, S., Laurell, E. and Kutay, U. (2009). Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat. Rev. Mol. Cell Biol. 10, 178-191.
13. Harborth, J., Wang, J., Gueth-Hallonet, C., Weber, K. and Osborn, M. (1999). Self assembly of NuMA: multiarm oligomers as structural units of a nuclear lattice. EMBO J. 18, 1689-1700.
14. Hutchison, C. J. (2002). Lamins: building blocks or regulators of gene expression? Nat. Rev. Mol. Cell Biol. 3, 848-858.
15. Kiyomitsu, T. and Cheeseman, I. M. (2012). Chromosome- and spindle-polederived signals generate an intrinsic code for spindle position and orientation. Nat. Cell Biol. 14, 311-317.
16. Kozlowski, C., Srayko, M. and Nedelec, F. (2007). Cortical microtubule contacts position the spindle in C. elegans embryos. Cell 129, 499-510.
17. Laan, L., Pavin, N., Husson, J., Romet-Lemonne, G., van Duijn, M., López, M. P., Vale, R. D., Jülicher, F., Reck-Peterson, S. L. and Dogterom, M. (2012). Cortical dynein controls microtubule dynamics to generate pulling forces that position microtubule asters. Cell 148, 502-514.
18. Lancaster, O. M. and Baum, B. (2011). Might makes right: using force to align the mitotic spindle. Nat. Cell Biol. 13, 736-738.
19. Luxenburg, C., Amalia Pasolli, H., Williams, S. E. and Fuchs, E. (2011). Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation. Nat. Cell Biol. 13, 203-214.
20. Margalit, A., Segura-Totten, M., Gruenbaum, Y. andWilson, K. L. (2005). Barrierto- autointegration factor is required to segregate and enclose chromosomes within the nuclear envelope and assemble the nuclear lamina. Proc. Natl. Acad. Sci. USA 102, 3290-3295.
21. Markus, S. M. and Lee,W.-L. (2011). Microtubule-dependent path to the cell cortex for cytoplasmic dynein in mitotic spindle orientation. Bioarchitecture 1, 209-215.
22. Mekhail, K. and Moazed, D. (2010). The nuclear envelope in genome organization, expression and stability. Nat. Rev. Mol. Cell Biol. 11, 317-328.
23. Orjalo, A. V., Arnaoutov, A., Shen, Z., Boyarchuk, Y., Zeitlin, S. G., Fontoura, B., Briggs, S., Dasso, M. and Forbes, D. J. (2006). The Nup107-160 nucleoporin complex is required for correct bipolar spindle assembly. Mol. Biol. Cell 17, 3806-3818.
24. Pekovic, V., Harborth, J., Broers, J. L. V., Ramaekers, F. C. S., van Engelen, B., Lammens, M., von Zglinicki, T., Foisner, R., Hutchison, C. and Markiewicz, E. (2007). Nucleoplasmic LAP2a-lamin A complexes are required to maintain a proliferative state in human fibroblasts. J. Cell Biol. 176, 163-172.
25. Puente, X., Quesada, V., Osorio, F. G., Cabanillas, R., Cadiñanos, J., Fraile, J. M., Ordóñez, G., Puente, D. A., Gutiérrez-Fernández, A., Fanjul-Fernández, M. et al. (2011). Exome sequencing and functional analysis identifies BANF1 mutation as the cause of a hereditary progeroid syndrome. Am. J. Hum. Gen. 88, 650-656.
26. Rosenblatt, J., Cramer, L. P., Baum, B. and McGee, K. M. (2004). Myosin II-dependent cortical movement is required for centrosome separation and positioning during mitotic spindle assembly. Cell 117, 361-372.
27. Scholey, J. M., Brust-Mascher, I. and Mogilner, A. (2003). Cell division. Nature 422, 746-752.
28. Simon, D. N. and Wilson, K. L. (2011). The nucleoskeleton as a genomeassociated dynamic 'network of networks'. Nat. Rev. Mol. Cell Biol. 12, 695-708.
29. Simon, D., Zastrow, M. S. and Wilson, K. L. (2010). Direct actin binding to A- and B-type lamin tails and actin filament bundling by the lamin A tail. Nucleus 1, 264-272.
30. Tsai, M.-Y.,Wang, S., Heidinger, J. M., Shumaker, D. K., Adam, S. A., Goldman, R. D. and Zheng, Y. (2006). A mitotic lamin Bmatrix induced by RanGTP required for spindle assembly. Science 311, 1887-1893.
31. Verlhac, M.-H. (2011). Spindle positioning: going against the actin flow. Nat. Cell Biol. 13, 1183-1185.
32. Verstraeten, V. L. R. M., Broers, J. L. V., Ramaekers, F. C. S. and van Steensel, M. A. M. (2007). The nuclear envelope, a key structure in cellular integrity and gene expression. Curr. Med. Chem. 14, 1231-1248.
33. Walczak, C. E. and Heald, R. (2008). Mechanisms of mitotic spindle assembly and function. Int. Rev. Cytol. 265, 111-158.
34. Weber, K. L., Sokac, A. M., Berg, J. S., Cheney, R. E. and Bement,W. M. (2004). A microtubule-binding myosin required for nuclear anchoring and spindle assembly. Nature 431, 325-329.
35. Wiese, C.,Wilde, A., Moore, M. S., Adam, S. A., Merdes, A. and Zheng, Y. (2001). Role of importin-beta in coupling Ran to downstream targets in microtubule assembly. Science 291, 653-656.
36. Wühr, M., Mitchison, T. J. and Field, C. M. (2008). Mitosis: new roles for myosin-X and actin at the spindle. Curr. Biol. 18, R912-R914.
37. Yao, C., Rath, U., Maiato, H., Sharp, D., Girton, J., Johansen, K. M. and Johansen, J. (2012). A nuclear-derived proteinaceous matrix embeds the microtubule spindle apparatus during mitosis. Mol. Biol. Cell 23, 3252-3541.
38. Yi, K., Unruh, J. R., Deng, M., Slaughter, B. D., Rubinstein, B. and Li, R. (2011). Dynamic maintenance of asymmetric meiotic spindle position through Arp2/3- complex-driven cytoplasmic streaming in mouse oocytes. Nat. Cell Biol. 13, 1252-1258.
39. Zheng, Y. (2010). A membranous spindle matrix orchestrates cell division. Nat. Rev. Mol. Cell Biol. 11, 529-535.
40. Zheng, R., Ghirlando, R., Lee, M. S., Mizuuchi, K., Krause, M. and Craigie, R. (2000). Barrier-to-autointegration factor (BAF) bridges DNA in a discrete, higherorder nucleoprotein complex. Proc. Natl. Acad. Sci. USA 97, 8997-9002.